Tansley review

Facilitation as a ubiquitous driver of biodiversity

Author for correspondence:Alex Fajardo

Tel: +56 67 2247821

Email: alex.fajardo@ciep.cl

Received: 25 May 2013

Accepted: 1 August 2013

Eliot J. B. McIntire1,2 and Alex Fajardo3

1Canadian Forest Service, Natural Resources Canada, 506 Burnside Road W., Victoria, BC, Canada, V8Z 1M5; 2Canada Research

Chair –Conservation Biology and Modeling, D�epartement des sciences du bois et de la foret, Universit�e Laval, Qu�ebec, QC, Canada;

3Centro de Investigaci�on en Ecosistemas de la Patagonia (CIEP) Conicyt–Regional R10C1003, Universidad Austral de Chile, Ignacio

Serrano 509, Coyhaique, Chile

Contents

Summary 403

I. Introduction 403

II. Facilitative mechanisms increasing diversity 405

III. Facilitation as an evolutionary driver in proximate interactions 410

IV. Why has facilitation been just recently addedto ecological theory? 411

V. Facilitation and the plant functional trait programme 412

VI. Predictability and testability 412

VII. Conservation, restoration and management 413

VIII. Conclusions and next steps 413

Acknowledgements 413

References 414

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Key words: biodiversity, coexistence,facilitation, intransitive competition, plantfunctional traits, positive interactions, resourcesharing, stress gradient hypothesis (SGH).

Summary

Models describing the biotic drivers that create and maintain biological diversity within trophic

levels have focused primarily on negative interactions (i.e. competition), leaving marginal room

for positive interactions (i.e. facilitation). We show facilitation to be a ubiquitous driver of

biodiversity byfirst noting that all species use resources and thus change the local biotic or abiotic

conditions, altering the available multidimensional niches. This can cause a shift in local species

composition,which can cause an increase in beta, and sometimes alpha, diversity.We show that

these increases are ubiquitous across ecosystems. These positive effects on diversity occur via a

broad host of disparate direct and indirect mechanisms. We identify and unify several of these

facilitative mechanisms and discuss why it has been easy to underappreciate the importance of

facilitation.Weshowthatnetpositive effects havea longhistoryofbeing consideredecologically

or evolutionarily unstable, and we present recent evidence of its potential stability. Facilitation

goes well beyond the common case of stress amelioration and it probably gains importance as

community complexity increases. While biodiversity is, in part, created by species exploiting

many niches, many niches are available to exploit only because species create them.

‘Simultaneous competition and beneficence [facilitation] can havemajor impacts on plant community structure’.

Hunter & Aarssen (1988)

‘…community assembly mechanisms determining the nature andmagnitude of facilitative effects on the composition of species anddiversity of a community are not well understood’.

Sch€ob et al. (2012)

I. Introduction

Interactions between organisms have long been considered a majordriver in the structuring and organization of natural communities(Hairston et al., 1960; Tilman, 1982; Mittelbach, 2012). Specif-ically, interactions within trophic levels have been widely deemedto be a key element of these drivers through their effect oncoexistence and biodiversity (Chesson, 2000; Silvertown, 2004).

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Review

Kropotkin (1902), Clements (1936), and Allee et al. (1949)showed that communities comprised a combination of positive andnegative interactions between species. As the paradigm withinwhich the field of ecology primarily operates is the struggle forexistence, negative interactions (e.g. competition) were repeatedlyfound to bemost important for species diversity, save for neutrality(Hubbell, 2001), in spite of calls and evidence to the contrary (e.g.Hay et al., 2004). The role of mutualisms in biodiversity – thoseinteractions that are traditionally identified as occurring betweenvery divergent evolutionary lines, such as mitochondria ineukaryotic cells, pollinators and plants, corals, mycorrhizas, andlichens, or very different trophic levels, such as cleaner fish–clientrelationships – is well known and widely appreciated (seemutualism chapters in recent editions of ecology texts, e.g. Cainet al., 2011; Mittelbach, 2012). Consequently, the focus of thispaper will be on the effects on biodiversity of positive interactionsamong same-trophic guilds, commonly referred to as facilitation,that have been dwarfed by the attention given to negativeinteractions (May, 1981; Gross, 2008).

Thework ofHunter&Aarssen (1988) can be considered the firstattempt to gather evidence on diverse types of positive plantinteractions, at the time called beneficence relationships.However, itwas not until the seminal work of Bertness & Callaway (1994) thatfacilitation was explicitly introduced as a biotic process that canhave important consequences in ecological communities, partic-ularly in stressful environments (i.e. the stress gradient hypothesis(SGH)). The SGH predicts that positive species interactions aremore important in biologically and physically stressful habitatsthan in benign habitats (Bertness&Callaway, 1994). Thereupon itcommenced a renaissance of experimental and observationalstudies focusing on the occurrence of facilitation and the testingof the SGH in a variety of apparently stressful systems, includingwater-stressed systems and alpine and salt marsh systems, whichrepeatedly supported the predictions of the SGH (Callaway, 2007;He et al., 2013). Facilitation has been defined as ‘an interaction inwhich the presence of one species alters the environment in a waythat enhances growth, survival and reproduction of a secondspecies’ (Bronstein, 2009). Although this definition appears tosynthesize well the original concept of facilitation and stressfulconditions (cf. Bertness&Callaway, 1994), it clearly does not limitfacilitation to stressful conditions (see Holmgren & Scheffer,2010). As such, several rapidly increasing bodies of ecological studyexamining positive interactions and their diverse modes of actionhave begun to suggest that facilitation may play more than just anincidental role in structuring plant communities through thealleviation of stressful conditions. Several reviews on facilitationhave been published (Callaway, 1995; Brooker et al., 2008;He et al., 2013) and new hypotheses have been proposed(Valiente-Banuet & Verd�u, 2007; Kikvidze & Callaway, 2009;McIntire&Fajardo, 2011; Soliveres et al., 2011) that together haveexpanded our understanding of the implications that facilitationhas for community ecology (Stachowicz, 2001; Bruno et al., 2003;Callaway, 2007; Brooker et al., 2008). Yet, in our opinion, thesereviews and new hypotheses still underestimate the role offacilitation in community ecology because they have primarilyfocused on the effects of individuals in creating obvious structures

and moderating abiotic stresses, which represent only a fraction ofthe mechanisms and ecosystems where facilitation actually occurs(cf. Callaway, 2007). That is, in spite of over 20 yr of intensiveresearch, and some attempts to include positive plant interactionsin ecological theory (e.g. Bruno et al., 2003; Michalet et al., 2006),within-trophic facilitation still appears to persist as a special casecontributor to the maintenance of species diversity, rather than aubiquitous driver of diversity at all scales. We believe that thispersistence is, first, a consequence of the clear importance ofantagonisms in simple experimental conditions and, secondly, aconsequence of the disparate mechanisms by which positiveinteractions occur, dissociating them from one another. As a result,the lack of unity linking the diverse mechanisms creating positivewithin-trophic effects on biodiversity may be at fault.

1. Facilitation, a ubiquitous process driving biodiversity

Until now, species have been perceived as resource users and thuscompetitors. While this is true, they are also, more generally,condition modifiers (Fig. 1). They change the distribution ofabiotic resources and change the biotic dynamics. Because allspecies’ niches differ across a different high-dimensional resourcespace and can be constrained by different high-dimensional factors,the new, local conditions will change the relative success of species,and favour a different array of species. For example, if a species useslight, it creates lower light conditions for all immediate neighboursgrowing beneath and changes the competitive hierarchies of thosespecies in the understory (e.g. shade-tolerants outcompete shade-intolerants); when a species uses nitrogen it locally reduces thenitrogen content and may change the carbon : nitrogen ratio,favouring different species; if a species ‘uses’ a generalist pollinator,itmay attractmore pollinators, encouraging pollen-limited species,and so on for all resources and conditions. The usual assumption isthat the use of resources has a negative effect on immediateneighbours. For community dynamics, however, it is not theabsolute sign of the effect, but the relative strength of that effect thatmatters. For example, stress- or shade-tolerant species may havereduced growth under stressful conditions or under a forest canopy,respectively, but their reduction is less than for stress- or shade-intolerant species, so new communities form (e.g. understorycommunities) from the local species pool. Thus, biodiversity can beincreased by any species presence through the modification of theavailable niches as compared to the abiotic environment alone, attimes increasing the alpha diversity and more generally increasingthe beta diversity (Fig. 1).

We define the facilitation effects on biodiversity as any increasein a diversity measure that results directly or indirectly from themodifications of biotic and abiotic conditions caused by any and allspecies’ presence. We spend the remainder of the text showingmany mechanisms by which these modifications occur and the vastdiversity of species on the planet that results from them. By doingthis, we unify a broad array of disparate mechanisms of net positivewithin-trophic interactions into the single ecological conceptknown as facilitation. Our proposed set of mechanisms is moreinclusive than that used in previous reviews and, as a result, wepresent evidence that facilitation is actually a major driver of

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biodiversity across ecosystems. These mechanisms include widelyknown drivers such as themitigation of abiotic stressors (e.g. SGH)and novel habitat creation, but also less widely appreciated ones,such as intransitive interactions, indirect interactions, being smallcompared to one’s neighbours, heterogeneity creation and resourcesharing. Indeed, many species modify conditions creating netpositive effects even in productive or nonstressful locations.

We structure our paper in six sections. First, we highlightempirical, analytical and simulation studies that show that a widerange of direct and indirectmechanisms change the biotic or abioticconditions and explicitly contribute to increase or maintaindiversity and are thus facilitative, and we highlight the partialduality between competition and facilitation as a result of indirecteffects. Secondly, we discuss briefly the importance of facilitationover evolutionary time and its evolutionary stability even underconditions that are considered unlikely from a strict understandingof competition. Thirdly, we discuss some reasons why this fullappreciation of positive effects has been overlooked until now.Fourthly, we examine new efforts at understanding facilitationusing plant functional traits. Fifthly, we discuss the predictabilityand testability of the different and disparate mechanisms of

facilitation that drive biodiversity, with particular reference to thetrait approach. Finally, we show why this understanding offacilitation can help in conservation, restoration and management.In this paper, we omit discussion of mutualisms because they arewidely known and appreciated. Similarly, we restrict our discussionto sessile organisms; however, all organisms change the localconditions, and we show several examples in tables and figures ofanimal facilitation. Rather, we focus on the ways in which positiveinteractions affect topics traditionally dominated by competitiverelationships and thus we constrain our discussion to same-trophiclevel net positive effects, consistentwith how facilitation is generallydefined (McIntire & Fajardo, 2011).

II. Facilitative mechanisms increasing diversity

All facilitative mechanisms act by benefactor species changing thebiotic or abiotic conditions for facilitated species. We highlightseveral known mechanisms and note that our particular classifica-tion of the mechanisms may not be mutually exclusive; that is,amelioration of stressful conditions could be conceived by some asnovel habitat creation. However, we present them to align with our

Novel habitat (e.g. forests, tussocks and salt marshes)

Indirect effects(e.g. competition

propagation and intransitivity)

Habitat complexity(e.g. smaller species and

spatial and temporal complexity)

Access to resources (e.g. grafting, hydraulic

lift and increaseddecomposition)

Stress amelioration (e.g. removal of constraints and improving conditions)

Service sharing(e.g. dispersal agents, shared

pollinators and plant defense guilds)

Site conditions without biotic drivers

Local conditions as modified by competition

Site conditions as modified by a facilitator

Local conditions as modified by competition and maximum possible facilitation effect (length of dashed arrow shows maximum facilitation effect; actual facilitation effect can be less, depending on case)

Individual species’fundamental niches

Site conditions with no facilitator

Fig. 1 Ability of facilitativemechanisms tomodify a site’s conditions created by the environment and by competition, allowing species diversity to change.Wedepict themultidimensional environmental conditionsat a sitewithoutbiotic drivers (dashedcircles) andmodifications to themproducedbybiotic drivers, eithercompetition alone (central green circle) or where facilitation and competition act together (outer green shapes). Small coloured circles represent themultidimensional niche requirements of a hypothetical sample of species, where colour is unique by species. The facilitator species is not depicted as it may ormaynot be at the same scale as the site (e.g. a treemodifies the site conditions below it anddoes not fully experience thosemodified conditions). At a given site,when competition alone is considered, available multidimensional conditions are a reduced subset of the environmental conditions (green circle is smaller thandashed circle). When facilitative mechanisms are added, local conditions will be shifted in a variety of ways depending on mechanisms (large arrows leadingoutwards from the large grey circle). For a species to occur, its niche requirementsmust be availablewithin the site conditions. Depending on themagnitude ofthe facilitative changes, new species may appear, previously present species may be lost, or some species will be maintained as their niche requirements arepresent, lost or maintained (appearance, disappearance or maintenance of small coloured circles). To show that facilitative drivers have the ability to push thesite conditions outside of themultidimensional space created by the abiotic environment alone, the green shapesmay extendwell outside of the dashed circles(e.g. novel habitat), depending on the strength of the particular facilitative mechanisms acting. The direction of the expansion of conditions is arbitrary. Forsimplicity, we omit biotic drivers other than competition and facilitation.

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historical understanding of facilitation. Furthermore, we updateand subsumeHunter &Aarssen’s (1988) nine types of, at the time,beneficiarymechanisms with new literature and new understandingof the mechanisms. Like competition (e.g. direct interferencecompetition and indirect exploitative and apparent competition),it is clear that facilitation encompasses both direct and indirectmechanisms. Facilitation may be complex and its indirect effectsmay be difficult to tease apart experimentally (Callaway, 2007, p.117). Yet, difficulty detecting such effects does not deny theirexistence; in many cases they can be well understood (Cz�ar�an et al.,2002; Brooker et al., 2008).

1. The direct mechanisms of facilitation

Positive interactions play a critical, but underappreciated, role in

ecological communities by reducing physical or biotic stresses in

existing habitats and by creating new habitats on which many species

depend

Stachowicz (2001)

We identify five broad mechanisms of direct facilitation asdrivers of diversity, of which two have dominated the literature(Fig. 1). These all cause changes in the biotic or abiotic conditions,altering the available multidimensional niches, allowing for

increased diversity (Hacker & Gaines, 1997; Michalet et al.,2006). The first two are stress amelioration and novel habitatcreation (Stachowicz, 2001; Callaway, 2007). Three others, lesscommonly associated with facilitation, are creation of habitatcomplexity, access to resources, and service sharing. For spaceconsiderations, we elaborate somewhat on only habitat complexityand resource sharing because they have recent additions in theliterature that provide new insights (Table 1; see citations thereinfor the others). We provide descriptions of types of service sharing(Table 1) and point to some literature on these. As these directmechanisms are the best understood in the literature and,furthermore, it is likely that ecologists will continue to identifyfurther mechanisms by which the biotic and abiotic changes to acommunity increase or maintain diversity, we limit the discussionhere.

First, in stress amelioration, the common situation is thatindividuals of species A ameliorate stressful conditions for individ-uals of species B, thus creating the niche requirements of the latter(Fig. 1; the green shape extends beyond environmental conditions).Consequently, the presence of species A (a nurse or foundationalplant) has positive net effects for species B. Formalized in the SGH,this process creates the conditions required by the facilitatedindividuals (Bruno et al., 2003; Brooker et al., 2008; Gross, 2008);in stressful environments facilitators allow more stress-intolerant

Table 1 The direct mechanisms of facilitation. Net positive effects of neighbouring species occur through changing the abiotic or biotic conditions, resulting inan alteration of site conditions for the facilitated species (Fig. 1)

Mechanism Example mechanisms Literature

Abiotic stressamelioration

Soil warming in cold or shading in hot conditions(e.g. stress gradient hypothesis; Fig. 2a)

Bertness & Callaway (1994), Bruno et al. (2003), Brooker et al. (2008),Soliveres et al. (2011)

Novel ecosystems Ecosystem engineers or ecosystem constructors (Fig. 2b)Structural support (Fig. 2c)Primary and secondary successionShade (e.g. forest understory)Niche construction

Connell & Slatyer (1977), Chapin et al. (1994), Jones et al. (1994),Odling-Smee et al. (2003), Badano et al. (2006), Brooker et al. (2008),Gedan & Bertness (2010), Kylafis & Loreau (2011),Lowman & Schowalter (2012)

Habitat complexity(heterogeneity)

Spatial and temporal complexity created by thephysical presence of speciesOrganism size and shape (e.g. larger speciesand species architecture)Accretion of soil organic matter

Tilman (1982), Pugnaire et al. (2004), Aarssen et al. (2006),Bartels & Chen (2010), Sch€ob et al. (2012)

Service sharing Pollination efficiency via interspecific mastingsynchrony (Fig. 3d)Animal dispersal efficiency via interspecificmasting synchronyPredator satiation (e.g. mixed species herds orflocks, and interspecific fruit masting)Social learning and transfer of information(e.g. about predation risks)Host defence overriding

Janzen (1974), Sinclair (1985), Kelly & Sork (2002), Shibata et al. (2002),Danchin et al. (2004), Sepp€anen et al. (2007), Smith et al. (2011)

Access to resources Keystone modifiersInterspecific social learning and transfer ofinformation about resources (e.g. habitatselection; Fig. 2d)Hydraulic liftDecomposition and nutrient cycling fromneighbouring plantsNeighbouring species regenerationResource sharing via bet-hedgingLow light, per se, in understories

Mills et al. (1993), Levine (1999), Nilsson &Wardle (2005),Zou et al. (2005), Li et al. (2007), McIntire & Fajardo (2011),Tarroux & DesRochers (2011), Uitdehaag (2011)

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species to persist (Fig. 2a,b; e.g. Butterfield et al., 2013). Severalstudies suggest that the impact of the SGH is probably underes-timated because we are only just realizing the implications of whatconstitutes a ‘relative’ stress gradient; stress is species-specific, itdoes not affect a community as a whole (K€orner, 2003), resulting instress-induced positive interactions being detected across widerthan expected gradients (Holmgren & Scheffer, 2010; Solivereset al., 2011). In the context of facilitation driving diversity, thebenefactor species used some array of resources, but concurrentlymodified the conditions such that the limiting resources, forexample moisture, were no longer limiting for its neighbours.

Secondly, under novel habitat creation, a number of species andspecies types alter the biotic or abiotic conditions in ways that arelarge enough that we chose to identify the new conditions as ‘novelhabitat’ (Fig. 1; the green shape can extend well outside ofenvironment). They have been called various names, includingecosystem constructors, ecosystem engineers and foundationspecies (Jones et al., 1994; Odling-Smee et al., 2003; Butterfieldet al., 2013). Within this category, there are well-known examples,such as corals, mangrove trees, salt marsh foundation species andcushion plants (Stachowicz, 2001; Bruno et al., 2003; Badanoet al., 2006), as well as other less appreciated examples, such as treesand giant kelps (e.g. Brooker et al., 2008). What was not fully

appreciated in these studies is that the effect of habitat creationoccurs at all scales, going well beyond the normal notions of ‘novelhabitat creation’. For example, plant species create spatial heter-ogeneity as a result of their spatial structures and resource usecreatingmore available niches for other species (Sch€ob et al., 2012).While these examples have enlarged our awareness of the ubiquityof stress amelioration and novel habitat creation, these are just twoof several mechanisms of facilitation.

Thirdly, according to the resource heterogeneity hypothesis,increasing habitat complexity for a given area increases the numberof species that can coexist, resulting in higher species diversity(Tilman, 1982; Mittelbach et al., 2001; Fig. 1; a shift in the greenshape, which can be quite complex). Often omitted, the source ofthe heterogeneity is commonly other species, which are thereforeproviding facilitative effects. Sch€ob et al. (2012) demonstrated thata key facilitative mechanism in their system was the creation ofheterogeneity, per se, distinct from niche space expansions andshifts. Similarly, nurse plants can increase the variability ofavailable niches (Soliveres et al., 2011). The mere presence ofrelatively large species, for example, can allow a higher diversityof physically small species as a result of heterogeneity creationby large plants (Aarssen et al., 2006). Furthermore, the creationof resource or sheltering heterogeneity may lead to an increase

(a) (b)

(c) (d)

Fig. 2 Some direct mechanisms of facilitation. (a) Plants can ameliorate stressful conditions for other plants, framed under the stress gradient hypothesis. Thephotograph shows Acacia caven (Fabaceae), which forms savannas in semi-arid regions of central Chile; under its canopy other species, such as Leucocoryneixioides (Liliaceae), Stellaria arvalis (Caryophyllaceae) andOlsynium junceum (Iridaceae), benefit from lower evapotranspiration. (b) Species create novelenvironments forother species, a process that sometimes involvesnurseplants (also ‘ecosystemengineers’ or ‘ecosystemconstructors’). Thephotograph showsthe alpine cushionAzorellamadreporica in the central AndesofChile,whichhostsmanyother species including (inset)Hordeumcomosum,Poa spp. (Poaceae)andLoasa sigmoidea (Loasaceae), species that survivepoorly outsideof cushions. (c) Structural support allowsnumerous speciesof vines andepiphytes to exist.The photograph shows Hydrangea serratifolia (Hydrangeaceae), a common vine in the Valdivian rainforest of Chile that grows on huge trees, such asAextoxicon punctatum (Aexotoxicaceae) and Eucryphia cordifolia (Cunoniaceae). (d) Interspecific social learning and transfer of information about predatorsis known to occur and increase survival. The photograph shows Eastern North America Carolina chickadee (Poecile carolinensis, in inset), which respondspositively to and clearly distinguishes the different predator threats encoded in titmouse (Baeolophus bicolor) calls they hear. Sources: (a) C. Torres, (b) A.Fajardo, (c) A. Salda~na and (d) Wikimedia commons.

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in niche segregation and competition intransitivity (see thesection on ‘The indirect mechanisms of facilitation’), which willultimately result in an increase of species richness (Tielb€orger &Kadmon, 2000; Soliveres et al., 2011).

Fourthly, individuals can also increase access to resources forother individuals via several mechanisms (Table 1; Fig. 1; this maycause the green shape to extend outside of environment). Themechanism of resource sharing, which appears to contradictexpectations based on competition, can occur directly (McIntire &Fajardo, 2011) or indirectly via mycorrhizas, for example (Simardet al., 1997). McIntire & Fajardo (2011) showed that otherwisecompeting trees (i.e. close neighbours) appeared to share resourcesthrough merging of woody tissues, with the result that mergedstems had higher survival and growth. Another similar exampleinvolves the transfer of phosphorus from one plant to another viamycorrhizal hyphae (Newman & Ritz, 1986; Simard et al., 1997)or raising the water table allowing access to deep water (Zou et al.,2005). While our study did not explain how this could beevolutionarily stable, Uitdehaag (2011) demonstrated mathemat-ically that resource sharing among competitors would occur as partof a bet-hedging strategy, particularly when conditions experiencedby the competitors are negatively correlated. The importance,therefore, of resource sharing would depend on the scale ofheterogeneity of resources. Overall, however, our understanding ofthis is weak and there is much room for theoretical advances here.

2. The indirect mechanisms of facilitation

If ‘webs’, ‘hierarchies’, or ‘loops’ of strong competitive effects within

communities can elicit strong positive indirect effects, then plant species

may be quite interdependent even though all pairwise interactions are

competitive

Callaway (2007)

Net positive effects can occur via compounding of multiplenegative effects, that is, indirect effects or ‘the enemyofmy enemy ismy friend’ (Table 2; Figs 1, 3). The emergence of these net positiveeffects throughmultiple negative proximate relationships has been,however, largely ignored in competition and facilitation research(but see Tielb€orger & Kadmon, 2000; Saccone et al., 2010;Soliveres et al., 2011). As a special case of indirect effects where thepairwise competition is asymmetric, intransitive competition –colloquially known as the ‘rock-paper-scissors’ model – andintransitive networks have also been recognized as having a majorrole in species coexistence (Levine, 1999; Cz�ar�an et al., 2002; Laird& Schamp, 2006; Allesina & Levine, 2011). Competitive intran-sitiveness is essentially a horizontal analogue of trophic cascades(Hairston et al., 1960) that can be more complex because thenetworks can be infinitely long through feedbacks on the self. It canallow individuals within a species to help each other (Thorpe et al.,2009), can promote coexistence (Laird & Schamp, 2009) and canprevent extinctions (Verd�u & Valiente-Banuet, 2008), and thefacilitation resulting from the intransitivitiesmay be themost likelyoutcome in complex systems (Allesina & Levine, 2011; E. J. B.McIntire, unpublished). An important intransitive competitivedriver is the greater relative strength of intraspecific competitioncompared with interspecific competition, well known as one of thecrucial premises for species coexistence stabilizingmechanisms thatmaintain species diversity (Chesson, 2000; Levine & HilleRis-Lambers, 2009).Newwork is showing that species diversitymay beincreased via intransitive competition because of multiple limitingfactors (Allesina & Levine, 2011). This mechanism effectivelyenhances and stabilizes species richness. While intransitive com-petition via the relative strength of intraspecific over interspecificcompetition can readily create positive effects and lead to theinclusion of more species in the community, the link to facilitationhas not been considered (Stachowicz, 2001; but seeGross, 2008) orhas been explicitly denied (p. 178 in Mittelbach, 2012).

Table 2 The intransitive processes of facilitation can create net positive effects that occur via compounding of multiple negative effects

Mechanism Description Literature

Competitive intransitiveness:the rock-paper-scissorsmodel

It is known that in both animals and plants competition networks withpairwise interactions between species are not transitive. This is like the‘rock-paper-scissor’ game applied to competition, with no universalscale of competitiveness. Of particular interest, competitively weakerspecies can persist because of this phenomenon (Fig. 3a,b), effectivelyreversing predictions of competitive exclusion niche models

Hairston et al. (1960), Levine (1999), Frean &Abraham (2001), Cz�ar�an et al. (2002),Verd�u & Valiente-Banuet (2008), Laird &Schamp (2009), Thorpe et al. (2009),Allesina & Levine (2011),Levi & Wilmers (2012)

Intraspecific competition Competitively dominant species are known to limit their ownabundances more than those of competitively inferior species, thusstabilizing coexistence; an individual of a given species competes withits spatially immediate conspecifics (high niche overlap), potentiallyreducing the growth of itself, encouraging the existence of immediateother-species neighbours (low niche overlap). This process is distinctfrom niche separation because it is the intraspecific competition thatdrives the coexistence, allowing species of relatively close niches tocoexist (Fig. 3c)

Chesson (2000), Levine &HilleRisLambers (2009)

Indirect effects When competition occurs and relationships are not fixed (i.e. species Amay outcompete species B under some conditions, but not others), thencompetition will propagate, creating indirect positive effects that arecomplex to evaluate. However, these indirect effects may be strongwhere species richness is high

Dethier & Duggins (1984), Vandermeer et al.(1985), Thompson et al. (1991),Levine (1999), E.J.B. McIntire, unpublished

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Indirect facilitation has been described for decades (Dethier& Duggins, 1984; Vandermeer et al., 1985; Levine, 1999), butits importance has been unclear because it has been difficult toidentify its effects empirically. Also, there has been no nullexpectation in the sign of a multitude of direct competitiveeffects. In a recent study (E. J. B. McIntire, unpublished), it wasshown that indirect facilitation via the propagation of negativecompetitive effects is indeed the null expectation of many netnegative interactions. Distinct from intransitive networks, it wasshown that this positive net effect also occurred even wherecompetitive relationships were not fixed (i.e. could changeaccording to context) and even where species were indistin-guishable (E. J. B. McIntire, unpublished), a situation that mayexist according to the neutral theory of biodiversity (Hubbell,2001). In these cases, it was sufficient that variation exist amongindividuals for diversity to be increased, consistent with Clark(2010), as a consequence of stochasticity. In this case, however,the mechanism occurred via the propagation of the negativeeffects. Where species niche requirements differed, richness wasincreased as a result of the well-known ratio of intraspecific tointerspecific competition (Chesson, 2000). Even here, however,individual variation further enhanced the species richness in

those conditions, particularly with a diverse species pool (E. J.B. McIntire, unpublished).

Indirect and intransitive facilitation undermines the identity offacilitation as a strict opposite to competition. Indeed, ifcompetition networks result in net positive effects as a result ofcompetitive mechanisms, such as resource exploitation, then theyare both competitive and facilitative. It is unclear, at the moment,whether indirect competition or intransitivity can change the siteconditions outside of those of the environment (Fig. 1; the greenshape does not extend beyond environment) or whether thatwould only occur via the compounding of indirect and directmechanisms (e.g. access to resources combined with indirectcompetition). Recent work on the relative prominence of indirectcompetition that increases diversity suggests that positive effectsare the most likely outcome of intransitive competitive networks(Allesina & Levine, 2011). The experimental and empiricalsupport for the importance of indirect and intransitive effects isgrowing rapidly, but it is nevertheless proving a challenge. As withother efforts in science, difficulty in measuring does notundermine the importance of the process; our challenge is todesign new tests of these hypotheses that are capable of detectingtheir importance.

(a) (b)

(c) (d)

Fig. 3 Examples of species and ecosystemswhere positive effects are likely common. (a) Tropical forests have several facilitative processes contributing to highbiodiversity. First, trees are ‘ecosystem constructors’ creating structures for species types including vines and epiphytes. Trees also create shade allowing theproliferation of shade-tolerant species, a massive collection of species that exists as a result of the net positive balance between the direct negative effects ofcanopy shading and the indirect positive effects of canopy shading on non-shade-tolerants. Furthermore, these forests are probably comprised of largeintransitive competition networks which result in net positive effects on species and biodiversity. The picture shows a tropical forest in Martinique, in theCaribbean Sea. (b) Shade-tolerantMyrceugenia planipes (Myrtaceae) growing under the dense canopy of the Valdivian rainforest of southern Chile. (c)Intraspecific competition occurring in ameadow in the French Alps (Vanoisemassif, Pralognan la Vanoise) probably enhances species richness, allowingmanyspecies, including Eryngium alpinum (Apiaceae), Campanula barbata (Campanulaceae) and Festuca paniculata (Poaceae), to coexist. (d) Masting speciessometimes have synchronized flowering across species (community masting), conveying mutual benefits via predator satiation; the picture shows a mixedtemperate deciduous Japanese forest of Fagus crenata (small seedling in the right inset) and Castanea crenata (fruits in the inset). Sources: (a, d) Wikimediacommons, (b) A. Fajardo, and (c) I. Till-Bottraud.

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III. Facilitation as an evolutionary driver in proximateinteractions

Positive interactions are important in evolutionary time, asdemonstrated by the existence of widespread species groups andecosystems in which facilitation is important (Table 3). Lortie et al.(2004) synthesized the findings of numerous studies showing thatinterdependence in communities, some adaptively based, isubiquitous, introducing the integrated community concept.Furthermore, invasional meltdown, where pre-existing positiverelationships are recreated in a new ecosystem, sometimes increas-ing or stabilizing diversity, attests to the importance of facilitationover large scales (Adams et al., 2003; Simberloff, 2006). A recentstudy showed that facilitative relationships among ‘competitors’can be selected for on very short time and spatial scales in aridenvironments as climate starts to shift (K�efi et al., 2008). In thiscase, the selection occurred primarily in species that only had shortdistance dispersal capabilities. In another study, stem merging wasshown to occur readily between spatial neighbours of the samespecies (McIntire&Fajardo, 2011), a phenomenon that caused theindividuals to avoid the ubiquitous transition from facilitative tocompetitive processes over ontogenetic time. In the context ofnatural selection, the trait allowing merging – and its possible linkto origins of plant grafting –was probably selected for because of the

dramatic increase in individual-level survival enjoyed within themerged groups (McIntire & Fajardo, 2011).

The obvious question about this latter type of positive interac-tion is: wouldn’t a cheater that takes resources from merged stems,but does not give back, win out? An earlier simulation study gave apossible answer to this question: within a world of cheaters, closecompetitors, and variable environments, both cheater and facili-tators can be selected for and be readily maintained depending onthe abiotic environment (Travis et al., 2005). In other words, thereare probably cheaters throughout the system, but the cheater doesnot take over under some, maybe many, conditions. If, in ahypotheticalworld, individualswithin a species could only be takersor givers, then takers wouldwin. In the real world, the two strategiescan co-exist within a population. Other factors that may reduce theimpact of cheating in facilitative interactions are related to partnerfidelity and partner choicemechanisms, like in mutualism (Axelrod& Hamilton, 1981; Simms et al., 2006).

Interestingly, another study showed that recent species lineagesconserve the regeneration niche (via nurse tree syndrome) of olderand distant lineages, showing that facilitation-induced biodiversitygains over evolutionary time were maintained (Valiente-Banuet &Verd�u, 2007). In such cases, facilitation is crucial in determiningcommunity composition by enhancing long-termbiodiversity. In arecent study, it has also been shown that alpine, foundational

Table 3 Species groups that are commonlyor near-obligate facilitators or benefactors (manyexamplesbelow fall undermore thanonedescription, allowing fora more comprehensive description of the prevalence of facilitation)

Species groups orecosystem type

Facilitatoror facilitated Description

Shade-tolerant species Facilitated Shade tolerance, defined as the ability to grow and survive in less than full-sunlight conditions, is a trait thatoccurs widely and is a key driver for a massive diversity of plants (Halpern & Spies, 1995; Fig. 3b).These species occur under the canopy of tall woody plants or algae, for example. They exist largely becausethe negative direct effects of canopy shading are weaker than the positive effects resulting from the sameshading on competitor species (Pages & Michalet, 2003). In most cases, shade-tolerant plant species areexcluded competitively when there is no shade provided by overstory species (Sher et al., 2002)

Keystone modifiers Facilitator Keystone modifiers, such as large herbivores or napped sapsuckers, provide resources for others of the sametrophic levels (Mills et al., 1993)

Parasitic species Facilitator With a role similar to that of some herbivores, parasitic plants may preferentially affect a competitive dominant,such as sandalwood (Santalum paniculatum), mistletoe (Viscum album), or Cuscuta salina (Callaway &Pennings, 1998), and thus lower its performance and increase species richness and coexistence(Watson, 2009)

Epiphytes and vines Facilitated These groups are near-obligate recipients of facilitative effects (although some vines grow on rocks or otherstructures; Fig. 2c). These include vast arrays of diversity including many mosses, lichens, ferns and othervascular plants (Sillett & Antoine, 2004). Lianas have recently been shown to support, and thus facilitate,themselves (Leicht-Young et al., 2011)

Forests, coral reefs,mangroves, salt marshes,and deserts asexample communities

Both Facilitation at the ecosystem level is ubiquitous. A large fraction of global biodiversity lives in ecosystems thatare entirely facilitative (Callaway, 2007)

Ecosystem engineers Facilitator Species such as corals, woody plants (e.g. trees), cushion plants (Fig. 2b) or algal forests (e.g. kelps) createstructures, and others, such as salt marsh founders, change conditions and create novel ecosystems(e.g. mangroves, coral reefs, and salt marshes) that otherwise would not exist. These are responsible forimportant changes to the abiotic environment, creating vast species diversity

Nurse plants Facilitator In many ecosystems, including alpine and arctic ecosystems, nurse plants create the sole substrate available forother plants to germinate and grow (Fig. 2b)

Communicating species Both Public information sharing among animals and even plants is known to be widespread, with large but unknowneffects on diversity (Danchin et al., 2004)

‘Smaller species’ Facilitated Because of the structural heterogeneity produced by larger species in a community, there is a greater diversityof small species than would otherwise exist (Aarssen et al., 2006; Bartels & Chen, 2010)

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cushion species have functioned asmicro-refugia by facilitating lessstress-tolerant lineages in severe environments world-wide(Butterfield et al., 2013).

IV. Why has facilitation been just recently added toecological theory?

From Gause’s day [1934] onward, the discussion of coexistence and

community assembly rules has been framed almost exclusively in terms of

competition, despite numerous but largely unsuccessful attempts to

broaden the discussion to include additional mechanisms.

Hubbell (2005)

1. The historical context

Because much of the 20th Century’s development of ecologicaltheory was firmly anchored in Darwin’s ‘struggle for existence’concept, the idea of antagonism between individuals through thepreponderance of negative density-dependence processes prevailedin the elaboration of models explaining species coexistence andbiodiversity. Lotka–Volterra’s model of interspecific competition,Gause’s competitive exclusion principle, and Hutchinson’s andMacArthur’s works on the multidimensional niche and limitedsimilarity are good examples of this, which were exclusively basedon negative interactions between species (Bruno et al., 2003;Mittelbach, 2012). According to Hubbell’s quote, ecologists havebeen preoccupiedwith a single explanation for species diversity (i.e.competition) and this has precluded us from conceiving other, alsoplausible, explanations of the ways in which patterns of speciesdiversity are shaped.

Concurrently, using a ‘facilitation’ version of the Lotka–Volterracompetitionmodel, Gause&Witt (1935) found that changing thesign of the interspecific effect models’ component from negative topositive tended ‘to lead to silly solutions in which both [facilitatorsand facilitated] populations undergo unbounded exponentialgrowth, in an orgy of mutual benefaction’ (reviewed inMittelbach,2012).Amongother things,webelieve that this silly result camefromkeeping the intraspecific density-dependent effect negative. Thisniche-similarity tenet of intraspecific negative density-dependentprocessmaybequestionedasauniversal lawinnaturalcommunities.A recent attempt to add explicit positive direct effects to this simplemodel showed quite a different result. Even though the individualpositive effects included were weaker than the individual negativeeffects, coexistence occurred as a result of the positive effects (Gross,2008). Supporting this point, in recent empirical studies, same-cohort conspecifics (i.e. strong niche overlap) did not compete butfacilitated each other’s survival (a cushion plant species in Cerfon-teyn et al., 2011; seedlings of a tree species in Fajardo &McIntire,2011; liana species in Leicht-Young et al., 2011; a biannual forbspecies in S. R. Biswas&H.H.Wagner, unpublished), challengingthe notion that individuals have to compete when they encounterother similar-niche individuals.These examples constitute evidencefor context-specific positive density dependence, with the samepattern seen in the Allee effect (Allee et al., 1949); that is, when thepopulation density is low, the addition of new individuals correlates

positively with individual fitness. In the case ofNothofagus pumilioseedlings(Fajardo&McIntire,2011), facilitationattheintraspecificlevel not only occurred at the establishment stage but continuedthrough later stand stages, including the self-thinning (i.e. maxi-mum competition) stage (McIntire & Fajardo, 2011). Introducingcontext specificity (i.e. low population size, abiotic stress, novelstructures, etc.) to intraspecific facilitation shines a new light on this80-yr-old model.

2. Is facilitation predisposed to be undetected?

In competition-focused research fields, such as ecology andeconomics, facilitation may be undetected because it appearsweaker than competitive mechanisms (Gross, 2008). Forthousands of years of human communities, sellers of goods whoare competing with one another have congregated inmarkets to sellto the public. Clearly, the individual sellers are competing with oneanother for the customer. But they are also facilitating each otherbecause they draw in purchasers that would otherwise beunavailable. In this case, these two mechanisms act at differentscales. If a researcher looks at direct interactions, there is clearlycompetition: the sellers are not giving each other anything directly.However, the entire stage on which the competition can occur is aresult of the facilitative interactions. It is also likely that there areindirect or intransitive effects occurring; having more competitorslimits you and your competitors, resulting in possible positiveeffects.

Under the niche paradigm, diversity is achieved by each speciesoccupying a unique combination of a multidimensional niche. Ifan ‘invader’ species arrives in the community, it may be able tothrive because there is a niche available (the empty nichehypothesis for invasion success; Stachowicz & Tilman, 2005).However, recent studies have demonstrated that the sameobservation can be caused by an undetected direct facilitativemechanism: organisms themselves increase the number of nichesby increasing habitat complexity (Sch€ob et al., 2012). In otherwords, are the species exploiting more niches, or are there moreniches to exploit? To differentiate these two mechanisms probablyrequires at least a trait-based analysis, which has only recently beenrelated to plant interactions (e.g. Sch€ob et al., 2012; Spasojevic &Suding, 2012; see the section on ‘Facilitation and the plantfunctional programme’). Unless explicitly evaluated and tested,the observations are identical whether the mechanism is abioticniche filling or heterogeneity creation via facilitation. In studiesaddressing intransitive competition, there are both competitiveand facilitative effects, and thus there will likewise be a detectionbias.

The abiotic stress amelioration may be the easiest facilitativemechanism to confirm because, at extreme drought or tempera-tures, species perish quickly in an experiment. If, in contrast, thefacilitative mechanism creates more heterogeneity allowing, say,more species covering a higher diversity of specific leaf area (SLA) tocoexist, the proximatemetric tomeasure is SLAdispersion, even if itis a coexistence mechanism and does lead eventually to greatersurvival of a greater diversity of species. The more readilymeasurable ‘metric’ of rapid experimental mortality creates a

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positive detection bias for tests of the SGH. Given that 20 yr agolittle was known about facilitation in stressful environments, andthat today we know that facilitation creates widespread productiv-ity and diversity increases virtually every time we look in theseenvironments, it is possible that facilitation via a variety ofmechanisms is widespread in all systems.

V. Facilitation and the plant functional traitprogramme

In recent years, myriad studies have focused on a plant functionaltrait programme,with themain goal being to understand how traitsmediate community assembly and coexistence and then to use thisunderstanding to predict the effects of global change on biodiver-sity (Suding et al., 2005). Functional trait research has shown thattrait variation creates fitness advantages through environmentalfiltering processes while simultaneously preventing competitiveexclusion via niche partitioning. Evidence for the latter comes fromthe great variation in trait values found within most communitiesand from studies showing that trait values of co-occurring speciesare overdispersed relative to expectations from null models (e.g.Westoby et al., 2002; Kraft et al., 2008). What has been lessexplored is that such within-community high trait dispersion maybe in part a result of facilitation (see Gross et al., 2009; Sch€ob et al.,2012; Spasojevic & Suding, 2012). There is growing evidence thatfacilitation also increases trait dispersion at the community level.Distinct from the overdispersion created by niche partitioning,under facilitation-driven overdispersion, the coexistence will be offunctionally contrasting species (e.g. Callaway, 2007; Gross et al.,2009; Butterfield & Briggs, 2011). Facilitator species (Table 3)mostly respond to abiotic environment filtering, so they possess thefunctional traits constrained by the environmental conditionsoccurring at larger scales than the community. In contrast,facilitated species mostly respond to biotic environment filteringrepresented by the modified conditions the facilitator speciesimposes, this being at a scale defined by the facilitator’s scope (i.e. abiotic environmental filter within a large-scale abiotic environ-mental filter). Thus, facilitated species will possess functional traitsaccording to these micro-scale conditions but not necessarily tothose found in the region: facilitator species’ positive effects notonly increase the number of species (see Butterfield et al., 2013) butalso increase trait dispersion in the local community (Gross et al.,2013; Fig. 1). Thus, distinguishing the cause of trait divergencewillrequire an understanding of the type of traits that occur; that is, themechanisms responsible for this trait divergence will reflect thefacilitation mechanisms outlined here.

Although existing work on trait-based approaches representsimportant advances in community ecology, it lacks predictivepower to understand the impact of any perturbation in commu-nity structuring. Thus, a shift from a phenomenological approachtowards a more mechanistic approach is currently needed andencouraged (Adler et al., 2013). Butterfield & Briggs (2011)experimentally found that, in an arid system, shrub speciesfacilitated by a nurse’s canopy showed functional traits related to aresource-conservative strategy but other colonizer species (nurse-independent) showed traits related to a more resource-acquisitive

strategy. Similarly, Sch€ob et al. (2012) found, in an alpine system,a significant trait differentiation between species facilitated bycushion species and others growing in bare ground: the formershowing a more resource-conservative strategy and the lattershowing a more resource-acquisitive strategy (higher leaf drymatter content (LDMC) and SLA). Although these studiesdemonstrate the functional causes and consequences of facilitationin community structuring, they also suggest that relevant traitsmay be idiosyncratic, that is, environment-dependent (Butterfield& Callaway, 2013). These examples of where studies havepursued the particular traits responsible for the patterns observedshow great promise in distinguishing facilitation-based traitdivergence from niche-based trait divergence. But it is with anunderstanding of all the mechanisms we have presented in thisstudy by which local environmental conditions and constraints aremodified that a functional understanding of facilitation willoccur.

VI. Predictability and testability

Testing this notion of facilitation as a driver of biodiversitywill havegreatest success if two things are achieved: (1) understanding theresource conditions, both at the site level and at the species level,and (2) allowing for indirect effects, either biotic (e.g. competitionpropagation) or abiotic (e.g. when changes in conditions causesome species to disappear but others to appear). Using a trait-basedapproach will help with both. For example, detecting a lowergrowth rate in a potential facilitated species as a result of the shadingfrom a ‘benefactor’ is not sufficient to reject the hypothesis offacilitation as a driver of biodiversity. In this case, if that lowergrowth rate in the shade is associated with the appearance of two ormore new species that are shade-tolerant, using a trait-basedapproach, facilitation has had its positive effect in increasingdiversity as predicted.

More specifically, each facilitative mechanism will require adifferent type of test. Some are well understood and are widelytested (e.g. primary succession and shade tolerance) and others arenot. Some have been testedmore recently and are becomingmatureand accepted hypotheses (e.g. SGH). Others, however, have onlyrecently been explored (e.g. nontransitive competition networks,hydraulic lift, resources sharing, and habitat complexity). Themoremature hypotheses have stronger predictions and have been widelysupported. Testing some of the less mature hypotheses may requiredifferent types of experiments from the traditional pairwisecompetitive trial.Mathematicalmodels of intransitive competitionare maturing and there are numerous alternative models thatprovide concrete predictions (e.g. Frean & Abraham, 2001; Laird&Schamp, 2009; E. J. B.McIntire, unpublished) that can be testedin controlled experiments. New work using traits to show themechanisms of facilitative interactions shows great promise (Sch€obet al., 2012). Other multi-species models indicate that the fractionof a community richness that comprises mutualistic versusexploitative relationships is greatest with low dispersal ability(Filotas et al., 2010), consistent with empirical work in arid systems(K�efi et al., 2008). However, resource sharing still has severalempirical observations (McIntire & Fajardo, 2011; Tarroux &

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DesRochers, 2011) but only two mathematical models that we areaware of that describe how it can persist on evolutionary time-scales(Travis et al., 2005; Uitdehaag, 2011).

Although species coexistence models based on niche theory haveprovided critical insights into how trade-offs (e.g. niche differences)can promote higher levels of species diversity, these insights havebeen mostly based on simple systems or experiments (e.g. twoannual species). In reality, these competition-based models haveprovided limited evidence for niche differences in more complexsystems (Clark, 2010), and have rarely provided general principlesabout many-species communities (Simberloff, 2004). Indeed,evidence suggests that competition-based models fail to explainspecies diversity in tropical forests where high numbers of specieswith very similar niches and life forms coexist. Likewise, incommunities subject to invasion, invaders without apparent nichedifferences are able to successfully establish (MacDougall et al.,2009). While there is some support for the neutral model in highlydiverse forests (Hubbell, 2001), there is also evidence rejecting theneutral model even in tropical forests (McGill et al., 2006; Ricklefs& Renner, 2012) and that there are coherence problems with thetheory (Clark, 2012). Further empirical tests that isolate individualmechanisms and that allow for detection of facilitativemechanismsare badly needed.

VII. Conservation, restoration and management

For a long time, intercropping systems, including agroforestry(Young, 1997), have been used to improve yield rates overmonocultures. Intercropping can increase yield rates through nichecomplementarity mechanisms but also via facilitative mechanismssuch as improved nutrient-use efficiency (Zhang & Li, 2003; Liet al., 2007). For conservation or restoration applications, thechallenge for practitioners is identifyingwhich positive interactionsare present, and how to take advantage of them to maintain orincrease biodiversity. In semi-arid and marine systems, facilitationis already being widely used in restoration (e.g. G�omez-Aparicioet al., 2004; Halpern et al., 2007), including recently appreciatedintraspecific facilitation (Madsen et al., 2012). These abiotic stressamelioration applications appear to be readily implementable withimmediate results. Climate or niche envelope approaches tounderstanding species responses to future climate lack bioticinteractions in general, and positive interactions as a rule.Successful predictions will probably require an understanding ofpositive interactions (Lortie et al., 2004). Promoting ecologicalresilience will look different if it is intransitive competitionnetworks that are promoting diversity. In a root grafting study(Tarroux et al., 2010), researchers may have resolved a major causeof ‘thinning shock’: trees whose neighbours are thinned mechan-ically show stagnant or declining growth (Vincent et al., 2009) andcan show high mortality rates (Harrington & Reukema, 1983), inspite of the increased space, light and access to nutrients. Newly cuttrees that were root-grafted converted the observed resource sharinginto resource sinks (Tarroux et al., 2010). But, as ecologists andland managers world-wide address ecosystem integrity, under-standing the potential positive effects in the system can change thestrategies used.

VIII. Conclusions and next steps

The unification under this single facilitation concept of severaldisparate mechanisms, which have previously been exploredseparately within the ecological literature, will create threebenefits in our effort to understand the structuring anddynamics of communities. First, the high relative importanceof positive effects on diversity in relation to negative effectsneeds to be better appreciated and explicitly studied withoutappealing to simplified communities that may bias the detectionof negative effects. Each time we depart from simple pairwiseinteraction frames of study, evidence is mounting that we willdetect positive effects as the net outcome in plant interactions.Thus, we can better explain and understand this type of resultand perform more appropriate studies if the null hypothesis ofcompetitive interactions is not strictly negative. Secondly, it iswrong to assume that negative effects are the only stable resultof plant interactions; there are numerous mechanisms that areevolutionarily stable that promote positive interactions withintrophic levels. By identifying processes and traits that drivepositive interactions it will become clear that positive effects areubiquitously stable. Thirdly, we demonstrated that facilitation isonly sometimes the opposite of competition, because facilitationinvolves net positive effects. The result of this enemy-of-my-enemy-is-my-friend phenomenon is net positive effects. Asthere is no absolute correct scale in ecology, both approaches arevalid and important. At times they act at the same scale (e.g.much of the SGH and intransitive competition), and at timesthey act at different scales (e.g. overstory trees facilitating shade-tolerant herbs which compete among themselves; Sch€ob et al.,2013). This result allows a deeper understanding of all themechanisms of positive effects in communities.

The importance of facilitation for diversity, includingintransitive and indirect mechanisms, is still unknown, althoughrecent evidence suggests that it may be particularly important inhigh-diversity ecosystems (Allesina & Levine, 2011; E. J. B.McIntire, unpublished). Few studies have attempted to quantifythe number of species that have been added to a communitybecause of facilitative interactions. Where it has been attempted,Hacker & Gaines (1997) estimated that at least 35% of theobserved species diversity in a salt marsh was present as a resultof direct facilitative interactions, Valiente-Banuet & Verd�u(2007) estimated that 90–100% of species of interest werefacilitated over evolutionary time, Stone & Roberts (1991)found that 20–40% of effects from direct competition werebeneficial in a simulation experiment, and E. J. B. McIntire(unpublished) found that indirect facilitation accounts for> 50% of species richness under a wide range of conditions.The number of species that would be classified as shadetolerant, an example which includes understory plants, and maybe the majority of the floristic diversity (Halpern & Spies,1995), would give an idea of the biodiversity consequences ofoverstory facilitation. As for the facilitative effects of competitiveintransitivity, there is an enormous potential biodiversity effectof this facilitation that may be responsible for a large fraction ofspecies in an ecosystem (Callaway, 2007). The challenge now is

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to quantify the relative importance of facilitative mechanismsfor maintaining global biodiversity by designing experimentsand studies that can, in principle, detect net positive interac-tions so that we can resolve questions such as: are the speciesexploiting more niches, or are they creating more niches toexploit?

Acknowledgements

Financial support came from the Centre d’�etudes de la foret (www.cef-cfr.ca) for a visiting scientist grant to A.F. and the CanadaResearch Chair program (EJBM). A.F. also acknowledges financialsupport from a FONDECYT Project No. 1120171. We alsoappreciate the help of A. Valiente-Banuet and P. Adler who kindlyreviewed a preliminary version of this paper. Finally, we thankA. Salda~na, I. Till-Bottraud and C. Torres for providing photo-graphs of their study sites.

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